This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Hanna, J. S.
Right arrow Articles by Spencer, F. A.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Hanna, J. S.
Right arrow Articles by Spencer, F. A.

 Previous Article  |  Next Article 

Molecular and Cellular Biology, May 2001, p. 3144-3158, Vol. 21, No. 9
0270-7306/01/$04.00+0   DOI: 10.1128/MCB.21.9.3144-3158.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.

Saccharomyces cerevisiae CTF18 and CTF4 Are Required for Sister Chromatid Cohesion

Joseph S. Hanna,1 Evgueny S. Kroll,2 Victoria Lundblad,3 and Forrest A. Spencer1,*

McKusick-Nathans Institute of Genetic Medicine, Johns Hopkins University School of Medicine, Baltimore, Maryland1; Molecular Sciences Institute, Berkeley, California2; and Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, Texas3

Received 4 December 2000/Returned for modification 17 January 2001/Accepted 8 February 2001

CTF4 and CTF18 are required for high-fidelity chromosome segregation. Both exhibit genetic and physical ties to replication fork constituents. We find that absence of either CTF4 or CTF18 causes sister chromatid cohesion failure and leads to a preanaphase accumulation of cells that depends on the spindle assembly checkpoint. The physical and genetic interactions between CTF4, CTF18, and core components of replication fork complexes observed in this study and others suggest that both gene products act in association with the replication fork to facilitate sister chromatid cohesion. We find that Ctf18p, an RFC1-like protein, directly interacts with Rfc2p, Rfc3p, Rfc4p, and Rfc5p. However, Ctf18p is not a component of biochemically purified proliferating cell nuclear antigen loading RF-C, suggesting the presence of a discrete complex containing Ctf18p, Rfc2p, Rfc3p, Rfc4p, and Rfc5p. Recent identification and characterization of the budding yeast polymerase kappa , encoded by TRF4, strongly supports a hypothesis that the DNA replication machinery is required for proper sister chromatid cohesion. Analogous to the polymerase switching role of the bacterial and human RF-C complexes, we propose that budding yeast RF-CCTF18 may be involved in a polymerase switch event that facilities sister chromatid cohesion. The requirement for CTF4 and CTF18 in robust cohesion identifies novel roles for replication accessory proteins in this process.

* Corresponding author. Mailing address: Johns Hopkins University School of Medicine, 720 Rutland Ave./Ross 850, Baltimore, MD 21205. Phone: (410) 614-2536. Fax: (410) 955-0484. E-mail: fspencer{at}jhmi.edu.

Molecular and Cellular Biology, May 2001, p. 3144-3158, Vol. 21, No. 9
0270-7306/01/$04.00+0   DOI: 10.1128/MCB.21.9.3144-3158.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.


This article has been cited by other articles:

  • Tanaka, H., Katou, Y., Yagura, M., Saitoh, K., Itoh, T., Araki, H., Bando, M., Shirahige, K. (2009). Ctf4 coordinates the progression of helicase and DNA polymerase {alpha}. GENES CELLS 14: 807-820 [Abstract] [Full Text]  
  • Celic, I., Verreault, A., Boeke, J. D. (2008). Histone H3 K56 Hyperacetylation Perturbs Replisomes and Causes DNA Damage. Genetics 179: 1769-1784 [Abstract] [Full Text]  
  • Ben-Shahar, T. R., Heeger, S., Lehane, C., East, P., Flynn, H., Skehel, M., Uhlmann, F. (2008). Eco1-Dependent Cohesin Acetylation During Establishment of Sister Chromatid Cohesion. Science 321: 563-566 [Abstract] [Full Text]  
  • Farina, A., Shin, J.-H., Kim, D.-H., Bermudez, V. P., Kelman, Z., Seo, Y.-S., Hurwitz, J. (2008). Studies with the Human Cohesin Establishment Factor, ChlR1: ASSOCIATION OF ChlR1 WITH Ctf18-RFC AND Fen1. J. Biol. Chem. 283: 20925-20936 [Abstract] [Full Text]  
  • Takahashi, T. S., Basu, A., Bermudez, V., Hurwitz, J., Walter, J. C. (2008). Cdc7-Drf1 kinase links chromosome cohesion to the initiation of DNA replication in Xenopus egg extracts. Genes Dev. 22: 1894-1905 [Abstract] [Full Text]  
  • Berkowitz, K. M., Kaestner, K. H., Jongens, T. A. (2008). Germline expression of mammalian CTF18, an evolutionarily conserved protein required for germ cell proliferation in the fly and sister chromatid cohesion in yeast. Mol Hum Reprod 14: 143-150 [Abstract] [Full Text]  
  • Biswas, D., Takahata, S., Xin, H., Dutta-Biswas, R., Yu, Y., Formosa, T., Stillman, D. J. (2008). A Role for Chd1 and Set2 in Negatively Regulating DNA Replication in Saccharomyces cerevisiae. Genetics 178: 649-659 [Abstract] [Full Text]  
  • Ansbach, A. B., Noguchi, C., Klansek, I. W., Heidlebaugh, M., Nakamura, T. M., Noguchi, E. (2008). RFCCtf18 and the Swi1-Swi3 Complex Function in Separate and Redundant Pathways Required for the Stabilization of Replication Forks to Facilitate Sister Chromatid Cohesion in Schizosaccharomyces pombe. Mol. Biol. Cell 19: 595-607 [Abstract] [Full Text]  
  • Hong, E. L., Balakrishnan, R., Dong, Q., Christie, K. R., Park, J., Binkley, G., Costanzo, M. C., Dwight, S. S., Engel, S. R., Fisk, D. G., Hirschman, J. E., Hitz, B. C., Krieger, C. J., Livstone, M. S., Miyasato, S. R., Nash, R. S., Oughtred, R., Skrzypek, M. S., Weng, S., Wong, E. D., Zhu, K. K., Dolinski, K., Botstein, D., Cherry, J. M. (2008). Gene Ontology annotations at SGD: new data sources and annotation methods. Nucleic Acids Res 36: D577-D581 [Abstract] [Full Text]  
  • Curcio, M. J., Kenny, A. E., Moore, S., Garfinkel, D. J., Weintraub, M., Gamache, E. R., Scholes, D. T. (2007). S-Phase Checkpoint Pathways Stimulate the Mobility of the Retrovirus-Like Transposon Ty1. Mol. Cell. Biol. 27: 8874-8885 [Abstract] [Full Text]  
  • Morton, C. O., Hayes, A., Wilson, M., Rash, B. M., Oliver, S. G., Coote, P. (2007). Global Phenotype Screening and Transcript Analysis Outlines the Inhibitory Mode(s) of Action of Two Amphibian-Derived, {alpha}-Helical, Cationic Peptides on Saccharomyces cerevisiae. Antimicrob. Agents Chemother. 51: 3948-3959 [Abstract] [Full Text]  
  • Hodgson, B., Calzada, A., Labib, K. (2007). Mrc1 and Tof1 Regulate DNA Replication Forks in Different Ways during Normal S Phase. Mol. Biol. Cell 18: 3894-3902 [Abstract] [Full Text]  
  • Pike, B. L., Heierhorst, J. (2007). Mdt1 Facilitates Efficient Repair of Blocked DNA Double-Strand Breaks and Recombinational Maintenance of Telomeres. Mol. Cell. Biol. 27: 6532-6545 [Abstract] [Full Text]  
  • Zhu, W., Ukomadu, C., Jha, S., Senga, T., Dhar, S. K., Wohlschlegel, J. A., Nutt, L. K., Kornbluth, S., Dutta, A. (2007). Mcm10 and And-1/CTF4 recruit DNA polymerase {alpha} to chromatin for initiation of DNA replication. Genes Dev. 21: 2288-2299 [Abstract] [Full Text]  
  • Skibbens, R. V., Maradeo, M., Eastman, L. (2007). Fork it over: the cohesion establishment factor Ctf7p and DNA replication. J. Cell Sci. 120: 2471-2477 [Abstract] [Full Text]  
  • Ogiwara, H., Ohuchi, T., Ui, A., Tada, S., Enomoto, T., Seki, M. (2007). Ctf18 is required for homologous recombination-mediated double-strand break repair. Nucleic Acids Res 35: 4989-5000 [Abstract] [Full Text]  
  • Xu, H., Boone, C., Brown, G. W. (2007). Genetic Dissection of Parallel Sister-Chromatid Cohesion Pathways. Genetics 176: 1417-1429 [Abstract] [Full Text]  
  • Vrouwe, M. G., Elghalbzouri-Maghrani, E., Meijers, M., Schouten, P., Godthelp, B. C., Bhuiyan, Z. A., Redeker, E. J., Mannens, M. M., Mullenders, L. H.F., Pastink, A., Darroudi, F. (2007). Increased DNA damage sensitivity of Cornelia de Lange syndrome cells: evidence for impaired recombinational repair. Hum Mol Genet 16: 1478-1487 [Abstract] [Full Text]  
  • Guacci, V. (2007). Sister chromatid cohesion: the cohesin cleavage model does not ring true. GENES CELLS 12: 693-708 [Abstract] [Full Text]  
  • Ogiwara, H., Ui, A., Enomoto, T., Seki, M. (2007). Role of Elg1 protein in double strand break repair. Nucleic Acids Res 35: 353-362 [Abstract] [Full Text]  
  • Andreassen, P. R., Ho, G. P.H., D'Andrea, A. D. (2006). DNA damage responses and their many interactions with the replication fork. Carcinogenesis 27: 883-892 [Abstract] [Full Text]  
  • Redon, C., Pilch, D. R., Bonner, W. M. (2006). Genetic Analysis of Saccharomyces cerevisiae H2A Serine 129 Mutant Suggests a Functional Relationship Between H2A and the Sister-Chromatid Cohesion Partners Csm3-Tof1 for the Repair of Topoisomerase I-Induced DNA Damage. Genetics 172: 67-76 [Abstract] [Full Text]  
  • Sabbioneda, S., Minesinger, B. K., Giannattasio, M., Plevani, P., Muzi-Falconi, M., Jinks-Robertson, S. (2005). The 9-1-1 Checkpoint Clamp Physically Interacts with Pol{zeta} and Is Partially Required for Spontaneous Pol{zeta}-dependent Mutagenesis in Saccharomyces cerevisiae. J. Biol. Chem. 280: 38657-38665 [Abstract] [Full Text]  
  • Archambault, V., Ikui, A. E., Drapkin, B. J., Cross, F. R. (2005). Disruption of Mechanisms That Prevent Rereplication Triggers a DNA Damage Response. Mol. Cell. Biol. 25: 6707-6721 [Abstract] [Full Text]  
  • Kim, J., Robertson, K., Mylonas, K. J. L., Gray, F. C., Charapitsa, I., MacNeill, S. A. (2005). Contrasting effects of Elg1-RFC and Ctf18-RFC inactivation in the absence of fully functional RFC in fission yeast. Nucleic Acids Res 33: 4078-4089 [Abstract] [Full Text]  
  • Bylund, G. O., Burgers, P. M. J. (2005). Replication Protein A-Directed Unloading of PCNA by the Ctf18 Cohesion Establishment Complex. Mol. Cell. Biol. 25: 5445-5455 [Abstract] [Full Text]  
  • Skibbens, R. V. (2005). Unzipped and loaded: the role of DNA helicases and RFC clamp-loading complexes in sister chromatid cohesion. JCB 169: 841-846 [Abstract] [Full Text]  
  • Losada, A., Hirano, T. (2005). Dynamic molecular linkers of the genome: the first decade of SMC proteins. Genes Dev. 19: 1269-1287 [Abstract] [Full Text]  
  • Tackett, A. J., Dilworth, D. J., Davey, M. J., O'Donnell, M., Aitchison, J. D., Rout, M. P., Chait, B. T. (2005). Proteomic and genomic characterization of chromatin complexes at a boundary. JCB 169: 35-47 [Abstract] [Full Text]  
  • Gygax, S. E., Semighini, C. P., Goldman, G. H., Harris, S. D. (2005). SepBCTF4 Is Required for the Formation of DNA-Damage-Induced UvsCRAD51 Foci in Aspergillus nidulans. Genetics 169: 1391-1402 [Abstract] [Full Text]  
  • Williams, D. R., McIntosh, J. R. (2005). Mcl1p Is a Polymerase {alpha} Replication Accessory Factor Important for S-Phase DNA Damage Survival. Eukaryot Cell 4: 166-177 [Abstract] [Full Text]  
  • Game, J. C., Williamson, M. S., Baccari, C. (2005). X-Ray Survival Characteristics and Genetic Analysis for Nine Saccharomyces Deletion Mutants That Show Altered Radiation Sensitivity. Genetics 169: 51-63 [Abstract] [Full Text]  
  • O'Neill, B. M., Hanway, D., Winzeler, E. A., Romesberg, F. E. (2004). Coordinated functions of WSS1, PSY2 and TOF1 in the DNA damage response. Nucleic Acids Res 32: 6519-6530 [Abstract] [Full Text]  
  • Antoniacci, L. M., Kenna, M. A., Uetz, P., Fields, S., Skibbens, R. V. (2004). The Spindle Pole Body Assembly Component Mps3p/Nep98p Functions in Sister Chromatid Cohesion. J. Biol. Chem. 279: 49542-49550 [Abstract] [Full Text]  
  • Zhou, Y., Wang, T. S.-F. (2004). A Coordinated Temporal Interplay of Nucleosome Reorganization Factor, Sister Chromatin Cohesion Factor, and DNA Polymerase {alpha} Facilitates DNA Replication. Mol. Cell. Biol. 24: 9568-9579 [Abstract] [Full Text]  
  • Xu, H., Boone, C., Klein, H. L. (2004). Mrc1 Is Required for Sister Chromatid Cohesion To Aid in Recombination Repair of Spontaneous Damage. Mol. Cell. Biol. 24: 7082-7090 [Abstract] [Full Text]  
  • Lee, M. S., Spencer, F. A. (2004). Bipolar orientation of chromosomes in Saccharomyces cerevisiae is monitored by Mad1 and Mad2, but not by Mad3. Proc. Natl. Acad. Sci. USA 101: 10655-10660 [Abstract] [Full Text]  
  • Petronczki, M., Chwalla, B., Siomos, M. F., Yokobayashi, S., Helmhart, W., Deutschbauer, A. M., Davis, R. W., Watanabe, Y., Nasmyth, K. (2004). Sister-chromatid cohesion mediated by the alternative RF-CCtf18/Dcc1/Ctf8, the helicase Chl1 and the polymerase-{alpha}-associated protein Ctf4 is essential for chromatid disjunction during meiosis II. J. Cell Sci. 117: 3547-3559 [Abstract] [Full Text]  
  • Askree, S. H., Yehuda, T., Smolikov, S., Gurevich, R., Hawk, J., Coker, C., Krauskopf, A., Kupiec, M., McEachern, M. J. (2004). From the Cover: A genome-wide screen for Saccharomyces cerevisiae deletion mutants that affect telomere length. Proc. Natl. Acad. Sci. USA 101: 8658-8663 [Abstract] [Full Text]  
  • Suter, B., Tong, A., Chang, M., Yu, L., Brown, G. W., Boone, C., Rine, J. (2004). The Origin Recognition Complex Links Replication, Sister Chromatid Cohesion and Transcriptional Silencing in Saccharomyces cerevisiae. Genetics 167: 579-591 [Abstract] [Full Text]  
  • Asthana, S., King, O. D., Gibbons, F. D., Roth, F. P. (2004). Predicting Protein Complex Membership Using Probabilistic Network Reliability. Genome Res 14: 1170-1175 [Abstract] [Full Text]  
  • Warren, C. D., Eckley, D. M., Lee, M. S., Hanna, J. S., Hughes, A., Peyser, B., Jie, C., Irizarry, R., Spencer, F. A. (2004). S-Phase Checkpoint Genes Safeguard High-Fidelity Sister Chromatid Cohesion. Mol. Biol. Cell 15: 1724-1735 [Abstract] [Full Text]  
  • Mayer, M. L., Pot, I., Chang, M., Xu, H., Aneliunas, V., Kwok, T., Newitt, R., Aebersold, R., Boone, C., Brown, G. W., Hieter, P. (2004). Identification of Protein Complexes Required for Efficient Sister Chromatid Cohesion. Mol. Biol. Cell 15: 1736-1745 [Abstract] [Full Text]  
  • Smolikov, S., Mazor, Y., Krauskopf, A. (2004). ELG1, a regulator of genome stability, has a role in telomere length regulation and in silencing. Proc. Natl. Acad. Sci. USA 101: 1656-1661 [Abstract] [Full Text]  
  • Baetz, K. K., Krogan, N. J., Emili, A., Greenblatt, J., Hieter, P. (2004). The ctf13-30/CTF13 Genomic Haploinsufficiency Modifier Screen Identifies the Yeast Chromatin Remodeling Complex RSC, Which Is Required for the Establishment of Sister Chromatid Cohesion. Mol. Cell. Biol. 24: 1232-1244 [Abstract] [Full Text]  
  • Skibbens, R. V. (2004). Chl1p, a DNA Helicase-Like Protein in Budding Yeast, Functions in Sister-Chromatid Cohesion. Genetics 166: 33-42 [Abstract] [Full Text]  
  • Lavoie, B. D., Hogan, E., Koshland, D. (2004). In vivo requirements for rDNA chromosome condensation reveal two cell-cycle-regulated pathways for mitotic chromosome folding. Genes Dev. 18: 76-87 [Abstract] [Full Text]  
  • Bellows, A. M., Kenna, M. A., Cassimeris, L., Skibbens, R. V. (2003). Human EFO1p exhibits acetyltransferase activity and is a unique combination of linker histone and Ctf7p/Eco1p chromatid cohesion establishment domains. Nucleic Acids Res 31: 6334-6343 [Abstract] [Full Text]  
  • Bermudez, V. P., Maniwa, Y., Tappin, I., Ozato, K., Yokomori, K., Hurwitz, J. (2003). The alternative Ctf18-Dcc1-Ctf8-replication factor C complex required for sister chromatid cohesion loads proliferating cell nuclear antigen onto DNA. Proc. Natl. Acad. Sci. USA 100: 10237-10242 [Abstract] [Full Text]  
  • Ben-Aroya, S., Koren, A., Liefshitz, B., Steinlauf, R., Kupiec, M. (2003). ELG1, a yeast gene required for genome stability, forms a complex related to replication factor C. Proc. Natl. Acad. Sci. USA 100: 9906-9911 [Abstract] [Full Text]  
  • Merkle, C. J., Karnitz, L. M., Henry-Sanchez, J. T., Chen, J. (2003). Cloning and Characterization of hCTF18, hCTF8, and hDCC1: HUMAN HOMOLOGS OF AN SACCHAROMYCES CEREVISIAE COMPLEX INVOLVED IN SISTER CHROMATID COHESION ESTABLISHMENT. J. Biol. Chem. 278: 30051-30056 [Abstract] [Full Text]  
  • Edwards, S., Li, C. M., Levy, D. L., Brown, J., Snow, P. M., Campbell, J. L. (2003). Saccharomyces cerevisiae DNA Polymerase {varepsilon} and Polymerase {sigma} Interact Physically and Functionally, Suggesting a Role for Polymerase {varepsilon} in Sister Chromatid Cohesion. Mol. Cell. Biol. 23: 2733-2748 [Abstract] [Full Text]  
  • Kenna, M. A., Skibbens, R. V. (2003). Mechanical Link between Cohesion Establishment and DNA Replication: Ctf7p/Eco1p, a Cohesion Establishment Factor, Associates with Three Different Replication Factor C Complexes. Mol. Cell. Biol. 23: 2999-3007 [Abstract] [Full Text]  
  • Bermudez, V. P., Lindsey-Boltz, L. A., Cesare, A. J., Maniwa, Y., Griffith, J. D., Hurwitz, J., Sancar, A. (2003). Loading of the human 9-1-1 checkpoint complex onto DNA by the checkpoint clamp loader hRad17-replication factor C complex in vitro. Proc. Natl. Acad. Sci. USA 100: 1633-1638 [Abstract] [Full Text]  
  • Chang, M., Bellaoui, M., Boone, C., Brown, G. W. (2002). A genome-wide screen for methyl methanesulfonate-sensitive mutants reveals genes required for S phase progression in the presence of DNA damage. Proc. Natl. Acad. Sci. USA 99: 16934-16939 [Abstract] [Full Text]  
  • Williams, D. R., McIntosh, J. R. (2002). mcl1+, the Schizosaccharomyces pombe Homologue of CTF4, Is Important for Chromosome Replication, Cohesion, and Segregation. Eukaryot Cell 1: 758-773 [Abstract] [Full Text]  
  • Warren, C. D., Brady, D. M., Johnston, R. C., Hanna, J. S., Hardwick, K. G., Spencer, F. A. (2002). Distinct Chromosome Segregation Roles for Spindle Checkpoint Proteins. Mol. Biol. Cell 13: 3029-3041 [Abstract] [Full Text]  
  • Garber, P. M., Rine, J. (2002). Overlapping Roles of the Spindle Assembly and DNA Damage Checkpoints in the Cell-Cycle Response to Altered Chromosomes in Saccharomyces cerevisiae. Genetics 161: 521-534 [Abstract] [Full Text]  
  • Lavoie, B. D., Hogan, E., Koshland, D. (2002). In vivo dissection of the chromosome condensation machinery: reversibility of condensation distinguishes contributions of condensin and cohesin. JCB 156: 805-815 [Abstract] [Full Text]  
  • Hirano, T. (2002). The ABCs of SMC proteins: two-armed ATPases for chromosome condensation, cohesion, and repair. Genes Dev. 16: 399-414 [Full Text]  
  • Wang, Z., Castano, I. B., Adams, C., Vu, C., Fitzhugh, D., Christman, M. F. (2002). Structure/Function Analysis of the Saccharomyces cerevisiae Trf4/Pol {sigma} DNA Polymerase. Genetics 160: 381-391 [Abstract] [Full Text]  
  • Lindsey-Boltz, L. A., Bermudez, V. P., Hurwitz, J., Sancar, A. (2001). Purification and characterization of human DNA damage checkpoint Rad complexes. Proc. Natl. Acad. Sci. USA 98: 11236-11241 [Abstract] [Full Text]  
  • Carson, D. R., Christman, M. F. (2001). Evidence that replication fork components catalyze establishment of cohesion between sister chromatids. Proc. Natl. Acad. Sci. USA 98: 8270-8275 [Abstract] [Full Text]  
  • Lavoie, B. D., Hogan, E., Koshland, D. (2002). In vivo dissection of the chromosome condensation machinery: reversibility of condensation distinguishes contributions of condensin and cohesin. JCB 156: 805-815 [Abstract] [Full Text]  


Copyright © 2009 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»